Skip to main content
Log in

Novel Chaperonins in a Prokaryote

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Group II chaperonins belong to the Hsp60 family occurring in archaea and eukaryotes. The archaeal chaperonins build the thermosome, which is similar to the eukaryotic CCT (chaperonin-containing TCP-1). Eukaryotes have eight subunits, and up until now, it was thought that archaea had between one and three subunits, depending on the species. We now report two novel subunits, termed Hsp60-4 and Hsp60-5, in the archaeon Methanosarcina acetivorans, which also has Hsp60-1, Hsp60-2, and Hsp60-3 with orthologs in Methanosarcinae. Hsp60-4 and Hsp60-5 occur only in M. acetivorans, which makes this organism unique in that it has the highest number of chaperonin subunits ever described for an archaeon. Evolutionary analysis suggests that either Hsp60-4 or Hsp60-5 paralogs have arisen by gene duplication with vastly increased accepted substitution rates or that they represent ancestral types found only in this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • JM Archibald AJ Roger (2002) ArticleTitleGene duplication and gene conversion shape the evolution of archaeal chaperonins J Mol Biol 316 1042–1050

    Google Scholar 

  • SF Altschul TL Madden AA Schaffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res 25 3389–3402 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694

    Article  CAS  PubMed  Google Scholar 

  • JM Archibald JM Logsdon SuffixJr WF Doolittle (1999) ArticleTitleRecurrent paralogy in the evolution of archaeal chaperonins Curr Biol 9 1053–1056 Occurrence Handle1:CAS:528:DyaK1MXmtlagsL0%3D Occurrence Handle10508614

    CAS  PubMed  Google Scholar 

  • JM Archibald C Blouin WF Doolittle (2001) ArticleTitleGene duplication and the evolution of group II chaperonins: Implications for structure and function J Struct Biol 135 157–169 Occurrence Handle1:CAS:528:DC%2BD3MXntFKqtbg%3D

    CAS  Google Scholar 

  • B Bukau E Deuerling C Pfund EA Craig (2000) ArticleTitleGetting newly synthesized proteins into shape Cell 101 119–122 Occurrence Handle1:CAS:528:DC%2BD3cXislKjurw%3D Occurrence Handle10786831

    CAS  PubMed  Google Scholar 

  • K Bustard RS Gupta (1997) ArticleTitleThe sequence of heat shock protein 40 (DnaJ) homologs provide evidence for a close evolutionary relationship between the Deinococcus-Thermus group and cyanobacteria J Mol Evol 45 193–205 Occurrence Handle1:CAS:528:DyaK2sXltFWltLk%3D Occurrence Handle9236279

    CAS  PubMed  Google Scholar 

  • E Conway de Macario AJL Macario (2003) ArticleTitleMolecular biology of stress genes in methanogens: Potential for bioreactor technology Adv Biochem Eng Biotechnol 81 95–150 Occurrence Handle1:CAS:528:DC%2BD3sXnvFalu70%3D Occurrence Handle12747562

    CAS  PubMed  Google Scholar 

  • E Conway de Macario DL Maeder AJL Macario (2003) ArticleTitleBreaking the mould: Archaea with all four chaperoning systems Biochem Biophys Res Commun 301 811–812 Occurrence Handle1:CAS:528:DC%2BD3sXhtVers7c%3D Occurrence Handle12589784

    CAS  PubMed  Google Scholar 

  • RJ Ellis SM Vies Particlevan der (1991) ArticleTitleMolecular chaperones Annu Rev Biochem 60 321–347 Occurrence Handle1:CAS:528:DyaK3MXmtVWitbk%3D Occurrence Handle1679318

    CAS  PubMed  Google Scholar 

  • JE Galagan et al. (2002) ArticleTitleThe genome of Methanosarcina acetivorans reveals extensive metabolic and physiological diversity Genome Res 12 532–542 Occurrence Handle1:CAS:528:DC%2BD38XivVemt74%3D Occurrence Handle11932238

    CAS  PubMed  Google Scholar 

  • S Geisler K Siegers E Schiebel (1998) ArticleTitleA novel protein complex promoting formation of functional alpha- and gamma-tubulin EMBO J 17 952–966 Occurrence Handle9463374

    PubMed  Google Scholar 

  • C Georgopoulos WJ Welch (1993) ArticleTitleRole of the major heat shock proteins as molecular chaperones Annu Rev Cell Biol 9 601–634 Occurrence Handle1:CAS:528:DyaK2cXntFKkuw%3D%3D Occurrence Handle8280473

    CAS  PubMed  Google Scholar 

  • Gish W (1996–2002) Wu Blast, http://blast.wustl.edu

  • MH Glickman A Ciechanover (2002) ArticleTitleThe ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction Physiol Rev 82 373–428 Occurrence Handle1:CAS:528:DC%2BD38XjtFOnsL4%3D Occurrence Handle11917093

    CAS  PubMed  Google Scholar 

  • S Gribaldo V Lumia R Creti E Conway de Macario A Sanangelantoni P Cammarano (1999) ArticleTitleDiscontinuous occurrence of the hsp70(dnaK) gene among archaea and sequence features of HSP70 suggest a novel outlook on phylogenies inferred from this protein J Bacteriol 181 434–443 Occurrence Handle1:CAS:528:DyaK1MXmtlWjsw%3D%3D Occurrence Handle9882656

    CAS  PubMed  Google Scholar 

  • RS Gupta (1995a) ArticleTitleEvolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells Mol Microbiol 15 1–11 Occurrence Handle1:CAS:528:DyaK2MXjtVWlurY%3D

    CAS  Google Scholar 

  • RS Gupta (1995b) ArticleTitlePhylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species Mol Biol Evol 12 1063–1073 Occurrence Handle1:CAS:528:DyaK2MXovVOis7g%3D

    CAS  Google Scholar 

  • RS Gupta (1998) ArticleTitleProtein phylogenies and signature sequences: A reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes Microbiol Mol Biol Rev 62 1435–1491 Occurrence Handle1:CAS:528:DyaK1MXhs1OntQ%3D%3D Occurrence Handle9841678

    CAS  PubMed  Google Scholar 

  • FU Hartl M Hayer-Hartl (2002) ArticleTitleMolecular chaperones in the cytosol: from nascent chain to folded protein Science 295 1852–1858 Occurrence Handle1:CAS:528:DC%2BD38XhvFClsL4%3D Occurrence Handle11884745

    CAS  PubMed  Google Scholar 

  • R Hengge B Bukau (2003) ArticleTitleProteolysis in prokaryotes: Protein quality control and regulatory principles Mol Microbiol 49 1451–1462 Occurrence Handle1:CAS:528:DC%2BD3sXnslKit74%3D Occurrence Handle12950913

    CAS  PubMed  Google Scholar 

  • J Hoehfeld DM Cyr C Patterson (2001) ArticleTitleFrom the cradle to the grave: Molecular chaperones may choose between folding and degradation EMBO Rep 21 885–890

    Google Scholar 

  • M Klumpp W Baumeister (1998) ArticleTitleThe thermosome: Archetype of group II chaperonins FEBS Lett 430 73–77 Occurrence Handle1:CAS:528:DyaK1cXktFGmu74%3D Occurrence Handle9678597

    CAS  PubMed  Google Scholar 

  • S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular Evolutionary Genetics Analysis software Bioinformatics 17 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    Article  CAS  PubMed  Google Scholar 

  • YP Kuo DK Thompson A St. Jean JR Charlebois CJ Daniels (1997) ArticleTitleCharacterization of two heat-shock genes from Haloferax volcanii: A model system for transcription regulation in the Archaea J Bacteriol 179 6318–6324 Occurrence Handle1:CAS:528:DyaK2sXmslOmt7w%3D Occurrence Handle9335278

    CAS  PubMed  Google Scholar 

  • S Lee ME Sowa Y Watanabe PB Sigler W Chiu M Yoshida TF Tsai (2003) ArticleTitleThe structure of ClpB: A molecular chaperone that rescues proteins from and aggregate state Cell 115 229–240 Occurrence Handle1:CAS:528:DC%2BD3sXosFCqsLk%3D Occurrence Handle14567920

    CAS  PubMed  Google Scholar 

  • MR Leroux M Faendrich D Klunker K Siegers AN Lupas JR Brown E Schiebel CM Dobson F-U Hartl (1999) ArticleTitleMtGimC, a novel archaeal chaperone related to the eukaryotic chaperonin cofactor GimC/prefoldin EMBO J 18 6730–6743 Occurrence Handle1:CAS:528:DC%2BD3cXhslyjsg%3D%3D Occurrence Handle10581246

    CAS  PubMed  Google Scholar 

  • G Levy-Rimler RE Bell N Ben-Tal A Azem (2002) ArticleTitleType I chaperonins: Not all are created equal FEBS Lett 529 1–5 Occurrence Handle1:CAS:528:DC%2BD38Xnt1Kktr0%3D Occurrence Handle12354603

    CAS  PubMed  Google Scholar 

  • DA Liberles (2001) ArticleTitleEvaluation of methods for determination of a reconstructed history of gene sequence evolution Mol Biol Evol 11 2040–2047

    Google Scholar 

  • AJL Macario M Lange BK Ahring E Conway Macario Particlede (1999) ArticleTitleStress genes and proteins in the Archaea Microbiol Mol Biol Rev 63 923–967 Occurrence Handle1:CAS:528:DC%2BD3cXjtVShsA%3D%3D Occurrence Handle10585970

    CAS  PubMed  Google Scholar 

  • AJL Macario M Malz E Conway de Macario (2004) ArticleTitleEvolution of assisted protein folding: The distribution of the main chaperoning systems within the phylogenetic domain Archaea Front Biosci 9 1318–1332 Occurrence Handle1:CAS:528:DC%2BD2cXhtFOktrg%3D Occurrence Handle14977547

    CAS  PubMed  Google Scholar 

  • DL Maeder (1999) CROSS: A Graphic Blast Cruncher, University of Maryland Biotechnology Institute Baltimore, MD

    Google Scholar 

  • JA Maupin-Furlow MA Gil IM Karadzic PA Kirkland CJ Reuter (2004) ArticleTitleProteasome: Perspectives from the Archaea Front Biosci 9 1743–1758 Occurrence Handle1:CAS:528:DC%2BD2cXlsFagsr0%3D Occurrence Handle14977583

    CAS  PubMed  Google Scholar 

  • AJ McClellan J Frydman (2001) ArticleTitleMolecular chaperones and the art of recognizing a lost cause Nat Cell Biol 3 E1–E3 Occurrence Handle11146635

    PubMed  Google Scholar 

  • A Mogk ED Deuerling S Vorderwuelbecke E Vierling B Bukau (2003) ArticleTitleSmall heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation Mol Microbiol 50 585–595 Occurrence Handle1:CAS:528:DC%2BD3sXoslKmt70%3D Occurrence Handle14617181

    CAS  PubMed  Google Scholar 

  • F Narberhaus (2002) ArticleTitleAlpha-crystallin-type heat-shock proteins: Socializing minichaperones in the context of a multichaperone network Microbiol Mol Biol Rev 66 64–93 Occurrence Handle1:CAS:528:DC%2BD38XislSntbk%3D Occurrence Handle11875128

    CAS  PubMed  Google Scholar 

  • FC Neidhardt RA Bogelen Particlevan V Vaughn (1984) ArticleTitleThe genetics and regulation of heat-shock proteins Annu Rev Genet 18 295–329 Occurrence Handle1:CAS:528:DyaL2MXktVOnsg%3D%3D Occurrence Handle6442118

    CAS  PubMed  Google Scholar 

  • BM Phipps A Hoffmann KO Stetter W Baumeister (1991) ArticleTitleA novel ATPase complex selectively accumulated upon heat shock is a major cellular component of thermophilic archaebacteria EMBO J 10 1711–1722 Occurrence Handle1:CAS:528:DyaK3MXltlWmtrs%3D Occurrence Handle1828761

    CAS  PubMed  Google Scholar 

  • NA Ranson HE White HR Saibil (1998) ArticleTitleChaperonins Biochem J 333 233–242 Occurrence Handle1:CAS:528:DyaK1cXltVylu7g%3D Occurrence Handle9657960

    CAS  PubMed  Google Scholar 

  • F Ritossa (1962) ArticleTitleA new puffing pattern induced by heat shock and DNP in Drosophila Experiential 8 571–573

    Google Scholar 

  • S Schlee P Beinker A Akhrymuk J Reinstein (2004) ArticleTitleA chaperone network for the resolution of protein aggregates: Direct interaction of ClpB and DnaK J Mol Biol 336 275–285 Occurrence Handle1:CAS:528:DC%2BD2cXkvFOmsg%3D%3D Occurrence Handle14741222

    CAS  PubMed  Google Scholar 

  • T Schwede J Kopp N Guex MC Peitsch (2003) ArticleTitleSWISS-MODEL: An automated protein homology-modeling server Nucleic Acids Res 31 3381–3385 Occurrence Handle1:CAS:528:DC%2BD3sXltVWjsLg%3D Occurrence Handle12824332

    CAS  PubMed  Google Scholar 

  • J Siltberg DA Liberles (2002) ArticleTitleA simple covarion-based approach to analyse nucleotide substitution rates J Evol Biol 15 588–594 Occurrence Handle1:CAS:528:DC%2BD38XlvFOhsro%3D

    CAS  Google Scholar 

  • P Srivastava (2002) ArticleTitleInteraction of heat shock proteins with peptides and antigen presenting cells: Chaperoning of the innate and adaptive immune responses Annu Rev Immunol 20 395–425 Occurrence Handle1:CAS:528:DC%2BD38XjtlWgtLo%3D Occurrence Handle11861608

    CAS  PubMed  Google Scholar 

  • K Strimmer A Haeseler Particlevon (1996) ArticleTitleQuartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies Mol Biol Evol 13 964–969 Occurrence Handle1:CAS:528:DyaK28XltlSmsLk%3D

    CAS  Google Scholar 

  • DK Thompson CJ Daniels (1998) ArticleTitleHeat-shock inducibility of and archaeal TATA-like promoter is controlled by adjacent sequence elements Mol Microbiol 27 541–551 Occurrence Handle1:CAS:528:DyaK1cXosValsg%3D%3D Occurrence Handle9489666

    CAS  PubMed  Google Scholar 

  • JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL_X Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 24 4876–4882 Occurrence Handle10.1093/nar/25.24.4876

    Article  Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • A Tissieres HK Mitchell UM Tracy (1974) ArticleTitleProtein synthesis in salivary glands of Drosophila melanogaster: Relation to chromosome puffs J Mol Biol 84 389–398 Occurrence Handle1:CAS:528:DyaE2cXks1Wgsr4%3D Occurrence Handle4219221

    CAS  PubMed  Google Scholar 

  • JD Trent E Nimmesgern JS Wall FU HartI AL Horwich (1991) ArticleTitleA molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide-1 Nature 354 490–493 Occurrence Handle1:CAS:528:DyaK3sXnsFGntA%3D%3D Occurrence Handle1836250

    CAS  PubMed  Google Scholar 

  • KN Truscott K Brandner N Pfanner (2003) ArticleTitleMechanism of protein import into mitochondria Curr Biol 13 R326–R337 Occurrence Handle1:CAS:528:DC%2BD3sXksVyiurc%3D Occurrence Handle12699647

    CAS  PubMed  Google Scholar 

  • IE Vainberg SA Lewis H Rommelaere C Ampe J Vandekerckhove HL Klein NJ Cowan (1998) ArticleTitlePrefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperon Cell 93 863–873 Occurrence Handle1:CAS:528:DyaK1cXjsl2ru7s%3D Occurrence Handle9630229

    CAS  PubMed  Google Scholar 

  • JM Valpuesta J Martin-Benito P Gomez-Puertas JL Carrascosa KR Willison (2002) ArticleTitleStructure and function of a protein folding machine: The eukaryotic cytosolic chaperonin CCT FEBS Lett 529 11–16 Occurrence Handle1:CAS:528:DC%2BD38Xnt1KktrY%3D Occurrence Handle12354605

    CAS  PubMed  Google Scholar 

  • KR Willison (1999) Composition and function of the eukaryotic cytosolic chaperonin-containing TCP-1 B Bukau (Eds) Molecular chaperones and folding catalysts Harwood Academic Publishers, Warwick Australia 555–571

    Google Scholar 

Download references

Acknowledgements

We are grateful to Mona Malz and Tara Garcia-Collins for their help and to the staff of the Photography and Illustration Unit of the Wadsworth Center for their expert assistance with the figures.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Everly Conway de Macario.

Additional information

Reviewing Editor: Dr. W. Ford Doolittle

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maeder, D.L., Macario, A.J. & de Macario, E.C. Novel Chaperonins in a Prokaryote. J Mol Evol 60, 409–416 (2005). https://doi.org/10.1007/s00239-004-0173-x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-0173-x

Keywords

Navigation